Abstract
Twitches are the unitary contractile events in both heart and skeletal muscles, but twitch plasticity in terms of force and the kinetics of force development differs considerably in the two muscle types. In skeletal muscle, twitch contractions are relatively invariant as long as temperature is constant and the muscle is well rested. In contrast, twitches in heart muscle exhibit much greater dynamic range, such that both force and the kinetics of force development can vary tremendously on a beat-to-beat basis. These differences are in part due to muscle-specific differences in the delivery of Ca2+ to the myoplasm during excitation-contraction coupling. In skeletal muscle, a single action potential elicits a transient increase in intracellular Ca2+ sufficient to saturate thin filament regulatory sites on troponin-C. Because of this, force development and the ability to do work depend upon the duration of the Ca2+ transient and therefore the time available for cross-bridge binding to actin, which in skeletal muscles can be prolonged by tetanic stimulation. In heart muscle, the increase in intracellular Ca2+ during a twitch is typically insufficient to saturate thin filament sites, so that twitch force and work production are sub-maximal. In contrast to skeletal muscle, cardiac muscle cannot be tetanized under physiological conditions, but twitch force and power can be varied by regulating the delivery of Ca2+ to the myoplasm and also by agonist-induced regulation of cross-bridge cycling kinetics.
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16.8. References
S. Schiaffino, and C. Reggiani, Molecular diversity of myofibrillar proteins: gene regulation and functional significance, Physiol. Rev. 76(2), 371–423 (1996).
A. M. Gordon, E. Homsher, and M. Regnier, Regulation of contraction in striated muscle, Physiol. Rev. 80(2), 853–924 (2000).
S. S. Lehrer, The regulatory switch of the muscle thin filament: Ca2+ or myosin heads, J. Muscle Res. Cell Motil. 15(3), 232–236 (1994).
R. J. Solaro, and H. M. Rarick, Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments, Circ. Res. 83(5), 471–480 (1998).
R. L. Moss, M. Razumova, and D. P. Fitzsimons, Myosin cross-bridge activation of cardiac thin filaments: implications for myocardial function in health and disease, Circ. Res. 94(10), 1290–1300 (2004).
S. Ebashi, and M. Endo, Calcium ion and muscle contraction, Prog. Biophys. Mol. Biol. 18, 123–183 (1968).
L. S. Tobacman, Thin filament-mediated regulation of cardiac contraction, Ann. Rev. Physiol. 58, 447–481 (1996).
J. S. Shiner, and R. J. Solaro, The Hill coefficient for the Ca2+-activation of striated muscle contraction, Biophys. J. 46(3), 541–543 (1984).
Z. Grabarek, J. Grabarek, P. C. Leavis, and J. Gergely, Cooperative binding to the Ca2+ specific sites of troponin C in regulated actin and actomyosin, J. Biol. Chem. 258(23), 14098–14102 (1983).
K. Guth, and J. D. Potter, Effect of rigor and cycling cross-bridges on the structure of troponin C and on the Ca2+ affinity of the Ca2+ specific regulatory sites in skinned rabbit psoas fibers, J. Biol. Chem. 262(28), 13627–13635 (1987).
R. D. Bremel, and A. Weber, Cooperation within actin filament in vertebrate skeletal muscle, Nature 238(5359), 97–101 (1972).
Z. Lu, R. L. Moss, and J. W. Walker, Tension transients initiated by photogeneration of MgADP in skinned skeletal muscle fibers, J. Gen. Physiol. 101(6), 867–888 (1993).
Z. Lu, D. R. Swartz, J. M. Metzger, R. L. Moss, and J. W. Walker, Regulation of force development studied by photolysis of caged ADP in rabbit skinned psoas fibers, Biophys. J. 81(1), 334–344 (2001).
H. Thirlwell, J. E. T. Corrie, G. P. Reid, D. R. Trentham, and M. A. Ferenczi, Kinetics of relaxation from rigor of permeabilized fast-twitch skeletal fibers from rabbit using a novel caged ATP and apyrase, Biophys. J. 67(6), 2346–2447 (1994).
J. A. Dantzig, M. G. Hibberd, D. R. Trentham, and Y. E. Goldman, Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibers, J. Physiol. 432(1), 639–680 (1991).
J. A. Dantzig, Y. E. Goldman, N. C. Millar, J. Lacktis, and E. Homsher, Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres, J. Physiol. 451(1), 247–278 (1992).
J. W. Walker, Z. Lu, and R. L. Moss. Effects of Ca2+ on the kinetics of phosphate release in skeletal muscle, J. Biol. Chem. 267(4), 2459–2466 (1992).
D. R. Swartz, and R. L. Moss, Influence of a strong-binding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers, J. Biol. Chem. 267(28), 20497–20506 (1992).
H. Nagashima, and S. Asakura, Studies on cooperative properties of tropomyosin-actin and tropomyosin-troponin-actin comples by the use of N-ethylmaleimide-treated and untreated species of myosin subfragment 1, J. Mol. Biol. 155(4), 409–428 (1982).
D. L. Williams, L. E. Greene, and E. Eisenberg, Cooperative turning on of myosin subfragment 1 adenosinetriphosphatase activity by the troponin-tropomyosin-actin complex, Biochemistry 27(18), 6987–6993 (1988).
D. P. Fitzsimons, J. R. Patel, K. S. Campbell, and R. L. Moss, Cooperative mechanisms in the activation dependence of the rate of force development in rabbit skinned skeletal muscle fibers, J. Gen. Physiol. 117(2), 133–148 (2001).
P. A. Hofmann, and F. Fuchs, Effect of length and cross-bridge attachment on Ca2+ binding to troponin C, Am. J. Physiol. 253(1), C90–C96 (1987).
F. Fuchs, and Y.-P. Wang, Force, length, and Ca2+-troponin C affinity in skeletal muscle, Am. J. Physiol. 261(5), C787–C792 (1991).
F. Fuchs, Mechanical modulation of the Ca2+ regulatory protein complex in cardiac muscle, NIPS 10, 6–12 (1995).
D. F. A. McKillop, and M. A. Geeves, Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament, Biophys. J. 65(2), 693–701 (1993).
K. Campbell, Rate constant of muscle force redevelopment reflects cooperative activation as well as crossbridge kinetics, Biophys. J. 72(1), 254–262 (1997).
C. A. Butters, J. B. Tobacman, and L. S. Tobacman, Cooperative effect of calcium binding to adjacent troponin molecules on the thin filament-myosin subfragment 1 MgATPase rate, J. Biol. Chem. 272(20), 13196–13202 (1997).
S. S. Lehrer, and M. A. Geeves, The muscle thin filament as a classical cooperative/allosteric regulatory System, J. Mol. Biol. 277(5), 1081–1089 (1998).
D. P. Fitzsimons, J. R. Patel, and R. L. Moss, Cross-bridge interaction kinetics in rat myocardium are accelerated by strong binding of myosin to the thin filament, J. Physiol. 530(2), 263–272 (2001).
B. Brenner, and E. Eisenberg, Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution, Proc. Natl. Acad. Sci. USA 83(10), 3542–3546 (1986).
B. Brenner, Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction, Proc. Natl. Acad. Sci. USA 85(9), 3265–3269 (1988).
A. Landesberg, and S. Sideman, Coupling calcium binding to troponin C and cross-bridge cycling in skinned cardiac cells, Am. J. Physiol. 266(3), H1260–H1271 (1994).
J. A. Dantzig, and Y. E. Goldman, Suppression of muscle contraction by vanadate, J. Gen. Physiol. 86(3), 305–327 (1985).
M. V. Razumova, A. E. Bukatina, and K. B. Campbell, Different myofilament nearest-neighbor interactions have distinctive effects on contractile behavior, Biophys. J. 78(6), 3120–3137 (2000).
K. Campbell, M. Chandra, R. D. Kirkpatrick, B. K. Slinker, and W. C. Hunter, Interpreting cardiac muscle force-length dynamics using a novel functional tool, Am. J. Physiol. 286(4), H1535–H1545 (2004).
M. Regnier, D. A. Martyn, and P. B. Chase, Calcium regulation of tension redevelopment kinetics with 2-deoxy-ATP or low [ATP] in skinned rabbit psoas fibers, Biophys. J. 74(4), 2005–2015 (1998).
P. W. Brandt, M. S. Diamond, and F. H. Schachat, The thin filament of vertebrate skeletal muscle cooperatively activates as a unit, J. Mol. Biol. 180(2), 379–384 (1984).
R. L. Moss, G. G. Giulian, and M. L. Greaser, The effects of partial extraction of TnC upon the tension-pCa relationship in rabbit skinned skeletal muscle fibers, J. Gen. Physiol. 86(4), 585–600 (1985).
M. R. Wolff, K. S. McDonald, and R. L. Moss, Rate of tension development in cardiac muscle varies with level of activator calcium, Circ. Res. 76(1), 154–160 (1995).
S. Palmer, and J. C. Kentish, Roles of Ca2+ and crossbridge kinetics in determining the maximum rates of Ca2+ activation and relaxation in rat and guinea pig skinned trabeculae, Circ. Res. 83(2), 179–186 (1998).
M. Regnier, H. Martin, R. J. Barsotti, A. J. Rivera, D. A. Martyn, and E. Clemmens, Cross-bridge versus thin filament contributions to the level and rate of force redevelopment in cardiac muscle, Biophys. J. 87(2), 1815–1824 (2004).
D. R. Manning, and J. T. Stull, Myosin light chain phosphorylation-dephosphorylation in mammalian skeletal muscle, Am. J. Physiol. 242(3), C234–C241 (1982).
W. G. Pyle, and R. J. Solaro, At the cross-roads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function, Circ. Res. 94(3), 296–305 (2004).
S. Miyata, W. Minobe, M. R. Bristow, and L. A. Leinwand, Myosin heavy chain isoform expression in the failing and nonfailing human heart, Circ. Res. 86(4), 386–390 (2000).
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Fitzsimons, D.P., Moss, R.L. (2007). Cooperativity in the Regulation of Force and the Kinetics of Force Development in Heart and Skeletal Muscles. In: Ebashi, S., Ohtsuki, I. (eds) Regulatory Mechanisms of Striated Muscle Contraction. Advances in Experimental Medicine and Biology, vol 592. Springer, Tokyo. https://doi.org/10.1007/978-4-431-38453-3_16
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DOI: https://doi.org/10.1007/978-4-431-38453-3_16
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